Antioxidant and Antibacterial Activity of Endophytic Fungi Isolated from The Leaves of Sungkai (Peronema canescens) http://www.doi.org/10.26538/tjnpr/v7i3.20
Main Article Content
Abstract
Sungkai (Peronema canescens) is a medicinal plant widely used in Indonesia. Its leaves are
believed to have the potential to treat fever and boost the immune system. This study investigated
the antioxidant and antibacterial activity of endophytic fungi extracts obtained from Sungkai
leaves. This will provide basic information for developing the potential of natural ingredients as
antioxidants and antibacterials. Endophytic fungi residing in Sungkai leaves were identified
morphologically. The antioxidant test was completed using DPPH, while the antibacterial activity
was tested using the paper disk diffusion method. Most potential endophytic fungal isolates were
identified through molecular identification, and the isolation of a bioactive compound was
achieved using column chromatography. The structure of the compound was determined using 1D
and 2D NMR spectroscopy methods. Four endophytic fungi isolates were observed in the Sungkai
leaves (code RND1–RND4). RND3 demonstrated very strong antioxidant activity (IC50 < 20
µg/mL) and strong antibacterial activity. Based on the molecular test, RND3 was identified as
Aspergillus niger. The pure compound isolated from RND3 revealed weak and strong antioxidant
(IC50 > 500 µg/mL) and antibacterial (MIC ≤ 64 µg/mL) properties, respectively. Spectroscopic
analysis showed that compound 1 was 3-benzyl-2,6-dihydroxy-1,4,11,13-tetramethyl-5-
methylene-12,15-dioxo-14-oxabicycloheptadeca-8,16-diene-7-carboxylic acid. Through further
research, this study can be used as a basis for the development of compounds as raw materials for
drugs.
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
References
Twaij BM, Hasan MN. Bioactive Secondary Metabolites from Plant Sources: Types, Synthesis, and Their Therapeutic
Uses. Int J Plant Biol. 2022; 13(1):4–14.
Agidew MG. Phytochemical analysis of some selected traditional medicinal plants in Ethiopia. Bull Natl Res Cent.
; 46(1):1-22.
Fitzgerald M, Heinrich M, Booker A. Medicinal plant analysis: A historical and regional discussion of emergent
complex techniques. Front Pharmacol. 2019; 10:1–14.
Navia ZI, Harmawan T, Suwardi ADIB. Ethnobotanical study of wild medicinal plants in Serbajadi protected forest of East Aceh District , Indonesia. 2022; 23(10):4959–70.
Khakurel D, Uprety Y, Ahn G, Cha JY, Kim WY, Lee SH. Diversity, distribution, and sustainability of traditional
medicinal plants in Kaski district, western Nepal. Front Pharmacol. 2022; 13:1–15.
Kunwar RM, Baral B, Luintel S, Uprety Y, Poudel RC, Adhikari B. Ethnomedicinal landscape: distribution of used
medicinal plant species in Nepal. J Ethnobiol Ethnome . 2022; 18(1):1–11.
Mahendradhata Y, Trisnantoro L, Listyadewi S, Soewondo P, MArthias T, Harimurti P. The Republic of Indonesia
Health System Review. 2017; 7(1):1-285.
Villena-Tejada M, Vera-Ferchau I, Cardona-Rivero A, Zamalloa-Cornejo R, Quispe-Florez M, Frisancho-Triveño
Z, Abarca-Melendez RC, Alvarez-Sucari SG, Mejia CR, Yanez JA. Use of medicinal plants for COVID-19 prevention
and respiratory symptom treatment during the pandemic in Cusco, Peru: A cross-sectional survey. PLoS One. 2021; 16(9): 1–18.
Odebunmi CA, Adetunji TL, Adetunji AE, Olatunde A, Oluwole OE, Adewale IA, Ejiwumi AO, Iheme CE, Aremu
TO. Ethnobotanical Survey of Medicinal Plants Used in the Treatment of COVID-19 and Related Respiratory Infections
in Ogbomosho South and North Local Government Areas, Oyo State, Nigeria. Plants. 2022; 11(19):1-27.
Latief M, Sari PM, Fatwa LT, Tarigan IL, Rupasinghe HPV. Antidiabetic Activity of Sungkai (Peronema canescens Jack)
Leaves Ethanol Extract on the Male Mice Induced Alloxan Monohydrate. Pharmacol Clin Pharm Res. 2021; 6(2):64-74.
Latief M, Tarigan IL, Sari PM, Aurora FE. Aktivitas Antihiperurisemia Ekstrak Etanol Daun Sungkai (Peronema canescens Jack) Pada Mencit Putih Jantan. Pharmacon J Farm Indones. 2021; 18(1): 23–37.
Pindan PN, Daniel, Chairul S, Rahayu A, Magdaleni. Uji Fitokimia Dan Uji Aktivitas Antioksidan Ekstrak Fraksi NHeksana, Etil Asetat Dan Etanol Sisa Dari Daun Sungkai (Peronema canescens Jack.) Dengan Metode Dpph. J At.
; 22–7.
Ibrahim A, Arifuddin M, Cahyo P W, Widayat W, Bone M. Isolation, Characterization and Secondary Metabolite
Endophytic Fungal Isolate From Peronema Canescens Jack Leaf and Coptosapelta tomentosa Val. K. Heyne Root. J Trop
Pharm Chem. 2019; 4(5): 215–25.
Aati HY, Anwar M, Al-Qahtani J, Al-Taweel A, Khan KUR, Aati S, Usman F, Ghallo BA, Asif HM, Shirazi JH, Abbasi
A. Phytochemical Profiling, In Vitro Biological Activities, and In-Silico Studies of Ficus vasta Forssk.: An Unexplored
Plant. Antibiotics. 2022; 11(9):1-26.
Rizwan K, Majeed I, Bilal M, Rasheed T, Shakeel A, Iqbal S. Phytochemistry and Diverse Pharmacology of Genus
Mimosa: A Review. Biomolecules. 2022; 12(1):1–31.
Magwilu KD, Nguta JM, Mapenay I, Matara D. Phylogeny, Phytomedicines, Phytochemistry, Pharmacological
Properties, and Toxicity of Croton gratissimus Burch (Euphorbiaceae). Adv Pharmacol Pharm Sci. 2022; 20(22):1-
Mir WR, Bhat BA, Rather MA, Muzamil S, Almilaibary A, Alkhanani M, Mir MA. Molecular docking analysis and
evaluation of the antimicrobial properties of the constituents of Geranium wallichianum D. Don ex Sweet from Kashmir
Himalaya. Sci Rep [Internet]. 2022; 12(1):1–17.
Al-Ishaq RK, Abotaleb M, Kubatka P, Kajo K, Büsselberg D. Flavonoids and their anti-diabetic effects: Cellular
mechanisms and effects to improve blood sugar levels. Biomolecules. 2019; 9(9): 1-35.
Méril-Mamert V, Ponce-Mora A, Sylvestre M, Lawrence G, Bejarano E, Cebrián-Torrejón G. Antidiabetic Potential of
Plants from the Caribbean Basin. Plants. 2022; 11(10): 1-23.
Elfita, Oktiansyah R, Mardiyanto, Widjajanti H, Setiawan A. Antibacterial and antioxidant activity of endophytic fungi
isolated from Peronema canescens leaves. Biodiversitas. 2022; 23(9):47-83.
Muharni M, Ferlinahayati F, Yohandini H, Riyanti F, Pakpahan Nap. The The Anticholesterol Activity Of Betulinic Acid And Stigmasterol Isolated From The Leaves Of Sungkai (Peronema canescens Jack). Int J Appl Pharm. 2021; 13(2): 198–203.
Kitagawa I, Simanjuntak P, Hori K, Nagami N, Mahmud T, Kobayashi M. Indonesian Medicinal Plants. VII. Seven New
Clerodane-Type Diterpenoids, Peronemins A2, A3, B1, B2, B3, C1, and D1, from the Leaves of Peronema canescens
(Verbenaceae). Chem Pharm Bull. 1994; 42(5): 10-50.
Sharifi-Rad M, Anil Kumar N V., Zucca P, Varoni EM, Dini L, Panzarini E, Rajkovic J, Fokou PVT, Azzini E, Peluso I, Mishra AP, Nigam M, Rayess YE, Beyrouthy ME, Polito L, Iriti M, Martins N, Martorell M, Docea AO, Setzer WN,
Calina D, Cho WC, Sharifi-Rad J. Lifestyle, Oxidative Stress, and Antioxidants: Back and Forth in the Pathophysiology of Chronic Diseases. Front Physiol. 2020; 11: 1–21.
Srinivasa C, Mellappa G, Patil SM, Ramu R, Shreevatsa B, Dharmashekar C, Kollur SP, Syed A, Shivamallu C. Plants
and endophytes–a partnership for the coumarin production through the microbial systems. Mycology [Internet]. 2022;1(1): 1–14.
Ashok A, Andrabi SS, Mansoor S, Kuang Y, Kwon BK, Labhasetwar V. Antioxidant Therapy in Oxidative StressInduced Neurodegenerative Diseases: Role of NanoparticleBased Drug Delivery Systems in Clinical Translation. Antioxidants. 2022; 11(2): 1-35.
Stoia M, Oancea S. Low-Molecular-Weight Synthetic Antioxidants: Classification, Pharmacological Profile,
Effectiveness and Trends. Antioxidants. 2022; 11(4):1-28.
Das P, Brahmachari G, Chatterjee K, Choudhuri T. Synthetic antioxidants from a natural source can overtake the
oncogenic stress management system and activate the stress ‑sensitized death of KSHV‑infected cancer cells. Int J Mol
Med. 2022; 50(3):1–18.
Dewage E, Sandun N, Nam K, Huang X, Ahn DU. Mechanisms , and Applications : A Review. 2022; 1(1): 1-
Sambu S, Hemaram U, Murugan R, Alsofi AA. Toxicological and Teratogenic Effect of Various Food Additives: An Updated Review. Biomed Res Int. 2022; 2022: 1-15.
Brockow K, Wurpts G, Trautmann A. Patients with questionable penicillin (beta-lactam) allergy: Causes and solutions. Allergol Sel. 2022; 6(01): 33–41.
Jourdan A, Sangha B, Kim E, Nawaz S, Malik V, Vij R, Sekhsaria S. Antibiotic hypersensitivity and adverse
reactions: Management and implications in clinical practice. Allergy, Asthma Clin Immunol [Internet]. 2020; 16(1):1–7.
Cruz JS, da Silva CA, Hamerski L. Natural products from endophytic fungi associated with rubiaceae species. J Fungi.
; 6(3):1–26.
dos Reis JBA, Lorenzi AS, do Vale HMM. Methods used for the study of endophytic fungi: a review on methodologies and challenges, and associated tips. Arch Microbiol [Internet]. 2022; 204(11):1–30.
Narayanan Z, Glick BR. Secondary Metabolites Produced by Plant Growth-Promoting Bacterial Endophytes.
Microorganisms. 2022; 10(10):1–18.
Alsharari SS, Galal FH, Seufi AM. Composition and Diversity of the Culturable Endophytic Community of Six
Stress-Tolerant Dessert Plants Grown in Stressful Soil in a Hot Dry Desert Region. J Fungi. 2022; 8(3):1-24.
Contreras-Cornejo HA, Macías-Rodríguez L, CortésPenagos C, López-Bucio J. Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in arabidopsis. Plant Physiol. 2020; 149(3):1579–92.
El-Sayed ESR, Hazaa MA, Shebl MM, Amer MM, Mahmoud SR, Khattab AA. Bioprospecting endophytic fungi for bioactive metabolites and use of irradiation to improve their bioactivities. AMB Express. 2022; 12(1):1-23.
Akter Y, Barua R, Uddin N, Muhammad Sanaullah AF, Marzan LW. Bioactive potentiality of secondary metabolites
from endophytic bacteria against SARS-COV-2: An in-silico approach [Internet]. Vol. 17, PLoS ONE. 2022; 1(1):1–37
Nzimande B, Kumalo HM, Ndlovu SI, Mkhwanazi NP. Secondary metabolites produced by endophytic fungi,
Alternaria alternata, as potential inhibitors of the human immunodeficiency virus. Front Genet. 2022; 13: 1–14.
Caruso DJ, Palombo EA, Moulton SE, Zaferanloo B. Exploring the Promise of Endophytic Fungi: A Review of Novel Antimicrobial Compounds. Microorganisms. 2022; 10(10):1-26.
El-Hawary SS, Moawad AS, Bahr HS, Abdelmohsen UR, Mohammed R. Natural product diversity from the
endophytic fungi of the genus Aspergillus. RSC Adv. 2020; 10(37):22058–79.
Santra HK, Banerjee D. Bioactivity study and metabolic profiling of Colletotrichum alatae LCS1, an endophyte of
club moss Lycopodium clavatum L. PLoS One [Internet]. 2022; 17: 1–29.
Aini K, Elfita E, Widjajanti H, Setiawan A. Bioactivity Endophytic Fungi Isolated from The Leaf Stalk of Syzygium
jambos. Trop J Nat Prod Res. 2022; 6(11):1765-1772.
Habisukan UH, Elfita, Widjajanti H, Setiawan A. Diversity of endophytic fungi in Syzygium aqueum. Biodiversitas.
; 22(3):1129–1137.
Syarifah, Elfita, Widjajanti H, Setiawan A, Kurniawati AR. Diversity of endophytic fungi from the root bark of yzygium
zeylanicum, and the antibacterial activity of fungal extracts, and secondary metabolite. Biodiversitas. 2021; 22(10):4572–
Fadhillah, Elfita, Muharni, Yohandini H, Widjajanti H. Chemical compound isolated from antioxidant active extract
of endophytic fungus Cladosporium tenuissimum in Swietenia mahagoni leaf stalks. Biodiversitas. 2019; 20(9):2645–50.
Abbas S, Shanbhag T, Kothare A. Applications of bromelain from pineapple waste towards acne. Saudi J Biol Sci
[Internet]. 2021; 28(1):1001–9.
Hapida Y, Elfita, Widjajanti H, Salni. Biodiversity and antibacterial activity of endophytic fungi isolated from jambu
bol (Syzygium malaccense). Biodiversitas. 2021; 22(12):5668–77.
Tamura K, Stecher G, Kumar S. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol Biol Evol.
; 38(7):3022–7.
Yu R, Liu J, Wang Y, Wang H, Zhang H. Aspergillus niger as a Secondary Metabolite Factory. Front Chem. 2021; 9: 1–
Chamilos G. crossm. Am Soc Microbiol. 2020;33(1):1–75.
Mousavi B, Hedayati MT, Hedayati N, Ilkit M, Syedmousavi S. Aspergillus species in indoor environments and their
possible occupational and public health hazards. Curr Med Mycol. 2016; 2(1): 36–42.
Lahlali R, Ezrari S, Radouane N, Kenfaoui J, Esmaeel Q, El Hamss H, Belabees Z, Barka A. Biological Control of Plant
Pathogens: A Global Perspective. Microorganisms. 2022; 10:1–33 p.
Silva PV, Pereira LM, de Souza Marques Mundim G, Maciel GM, de Araújo Gallis RB, de Oliveira Mendes G. Field
evaluation of the effect of Aspergillus niger on lettuce growth sing conventional measurements and a high-throughput
phenotyping method based on aerial images. PLoS One. 2022; 17(9): 1–14.
Garrigues S, Kun RS, Peng M, Bauer D, Keymanesh K, Lipzen A, Ng V, Grigoriev IV, de Vries RP. Unraveling the
regulation of sugar beet pulp utilization in the industriall relevant fungus Aspergillus niger. iScience [Internet]. 2022;
(4): 104065.
Mundim G de SM, Maciel GM, Mendes G de O. Aspergillus niger as a Biological Input for Improving Vegetable Seedling Production. Microorganisms. 2022; 10(4):674-721.
Chugh RM, Mittal P, MP N, Arora T, Bhattacharya T,Chopra H, Cavalu S, Gautam RK. Fungal Mushrooms: A Natural Compound With Therapeutic Applications. Frontiers in Pharmacology. 2022; 13(7):1–16.
Brazkova M, Angelova G, Mihaylova D, Stefanova P, Pencheva M, Gledacheva V, et al. Bioactive Metabolites
from the Fruiting Body and Mycelia of Newly-Isolated Oyster Mushroom and Their Effect on Smooth Muscle Contractile Activity. Foods. 2022; 11(24):1-29.
Rehman B, Khan SA, Hamayun M, Iqbal A, Lee IJ. Potent Bioactivity of Endophytic Fungi Isolated from Moringa
oleifera Leaves. Biomed Res Int. 2022; 20(22):246-1021.
Vaou N, Stavropoulou E, Voidarou CC, Tsakris Z. Interactions between Medical Plant-Derived BioactiveCompounds : Focus on Antimicrobial Combination Effects. 2022; 1–23.
Wei L, Zhang Q, Xie A, Xiao Y, Guo K, Mu S, Xie Y, Li z, He T. Isolation of Bioactive Compounds, Antibacterial Activity, and Action Mechanism of Spore Powder From Aspergillus niger xj. Frontiers in Microbiology. 2022; 13(7):1–13.
Stan D, Enciu AM, Mateescu AL, Ion AC, Brezeanu AC, Stan D, Tanase C. Natural Compounds With Antimicrobial
and Antiviral Effect and Nanocarriers Used for Their Transportation. Front Pharmacol. 2021; 12(9):1–25.
Rahimi NNMN, Ikhsan NFM, Loh JY, Ranzil FKE, Gina M, Lim SHE, Lai KS, Chong CM. Phytocompounds as an
Alternative Antimicrobial Approach in Aquaculture. Antibiotics. 2022; 11(4):1-19.
Mózsik L, Iacovelli R, Bovenberg RAL, Driessen AJM. Transcriptional Activation of Biosynthetic Gene Clusters in Filamentous Fungi. Front Bioeng Biotechnol. 2022; 10(7):1– 22.
Wang X, Lu Y, Shaaban KA, Wang G, Xia X, Zhu Y. Editorial: Bioactive Natural Products from Microbes: Isolation, Characterization, Biosynthesis and Structure Modification. Front Chem. 2022; 10(3):1–3.
Ndezo Bisso B, Njikang Epie Nkwelle R, Tchuenguem Tchuenteu R, Dzoyem JP. Phytochemical Screening, Antioxidant, and Antimicrobial Activities of Seven Underinvestigated Medicinal Plants against Microbial Pathogens. Adv Pharmacol Pharm Sci. 2022; 2022.
Mehmood A, Javid S, Khan MF, Ahmad KS, Mustafa A. In vitro total phenolics, total flavonoids, antioxidant and
antibacterial activities of selected medicinal plants using different solvent systems. BMC Chem [Internet]. 2022; 16(1):1–10.
Mapfumari S, Nogbou ND, Musyoki A, Gololo S, Mothibe M, Bassey K. Phytochemical Screening, Antioxidant and
Antibacterial Properties of Extracts of Viscum continuum E. Mey. Ex Sprague, a South African Mistletoe. Plants. 2022; 11(16):1-32.
El-Zahar KM, Al-Jamaan ME, Al-Mutairi FR, Al-Hudiab AM, Al-Einzi MS, Mohamed AAZ. Antioxidant, Antibacterial, and Antifungal Activities of the Ethanolic Extract Obtained from Berberis vulgaris Roots and Leaves. Molecules. 2022; 27(18):1-28.
Egorov AM, Ulyashova MM, Rubtsova MY. Bacterial Enzymes and Antibiotic Resistance. Acta naturae. 2018, 10(4): 33–48.
Roy R, Tiwari M, Donelli G, Tiwari V. Strategies for combating bacterial biofilms: A focus on anti-biofilm agents
and their mechanisms of action. Virulence. 2018; 9(1): 522– 54.
7Makarewicz M, Drożdż I, Tarko T, Duda-Chodak A. The interactions between polyphenols and microorganisms, especially gut microbiota. Antioxidants. 2021; 10(2): 1–70.
Ferraz CR, Carvalho TT, Manchope MF, Artero NA, Rasquel-Oliveira FS, Fattori V, Casagrande R, Verri WA.
Therapeutic potential of flavonoids in pain and inflammation: Mechanisms of action, pre-clinical and clinical data, and pharmaceutical development. Vol. 25, Molecules. 2020: 1(1):1–35.
Parcheta M, Świsłocka R, Orzechowska S, Akimowicz M, Choińska R, Lewandowski W. Recent developments in
effective antioxidants: The structure and antioxidant properties. Materials (Basel). 2021; 14(8):1–24.
Zheng YZ, Deng G, Liang Q, Chen DF, Guo R, Lai RC. Antioxidant activity of quercetin and its glucosides from
propolis: A theoretical study. Sci Rep. 2017; 7(1):1–11.
Sun Y, Ji X, Cui J, Mi Y, Zhang J, Guo Z. Synthesis, Characterization, and the Antioxidant Activity of Phenolic
Acid Chitooligosaccharide Derrivatives. Marine Drug. 2022; 1(1):16-48.
Kubiak-Tomaszewska G, Roszkowski P, Grosicka-Maciąg E, Strzyga-łach P, Struga M. Effect of Hydroxyl Groups Esterification with Fatty Acids on the Cytotoxicity and Antioxidant Activity of Flavones. Molecules. 2022; 27(2):1- 34.
Moazzen A, Öztinen N, Ak-Sakalli E, Koşar M. Structureantiradical activity relationships of 25 natural antioxidant
phenolic compounds from different classes. Heliyon. 2022; 8(9):1-21.
Skroza D, Šimat V, Vrdoljak L, Jolić N, Skelin A, Čagalj M, Frleta R, Mekinic IG. Investigation of Antioxidant Synergisms and Antagonisms among Phenolic Acids in the Model Matrices Using FRAP and ORAC Methods. Antioxidants. 2022; 11(9):1-15.
Okolie NP, Falodun A, Oluseyi D. Evaluation of the antioxidant activity of root extract of pepper fruit (Dennetia
tripetala), and its potential for the inhibition of Lipid peroxidation. Afr J. Trad Compl and Altern Med. 2014;
(3):221-227.
Charlton NC, Mastyugin M, Torok B, Torok M. Structural features of small molecule antioxidants and strategic
modifications to improve potential bioactivity. Molecules. 2023; 28(1):1-39